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Mechanisms of Song Perception in Oscine Birds Brain & Language 115 (2010) 59–68 Contents lists available at ScienceDirect Brain & Language journal homepage: www.elsevier.com/locate/b&l Mechanisms of song perception in oscine birds Daniel P. Knudsen a, Timothy Q. Gentner b,* a Neurosciences Graduate Program, University of California, San Diego, La Jolla, CA 92093, United States b Department of Psychology, University of California, San Diego, La Jolla, CA 92093, United States article info abstract Article history: Songbirds share a number of parallels with humans that make them an attractive model system for Accepted 23 September 2009 studying the behavioral and neurobiological mechanisms that underlie the learning and processing of Available online 14 May 2010 vocal communication signals. Here we review the perceptual and cognitive mechanisms of audition in birds, and emphasize the behavioral and neural basis of song recognition. Where appropriate, we point Keywords: out a number of intersections with human vocal communication behavior that suggest common mech- Psychoacoustics anisms amenable to further study, and limitations of birdsong as a model for human language. Auditory Ó 2010 Elsevier Inc. All rights reserved. Vocal communication Language Songbird Evolution Neuroethology Speech 1. Introduction tinuous stream of acoustic information as a collection of behavior- ally relevant communication signals and uses this information to Like other communication signals, one adaptive function of affect behavior (Fig. 1). Parallels will be drawn to human vocal birdsong is to influence the behavior of others, usually conspecific communication, and we will present a case for the use of songbirds individuals (Kroodsma & Miller, 1996). Communication signals as a model of certain aspects of human language processing. We achieve this function by transmitting information between the first provide a broad overview of perceptual psychophysics in sender of the signal and the receivers. The success of this transmis- songbirds so that one can appreciate the strong perceptual similar- sion rests on predictability. When a sender produces a specific sig- ities between birds and humans. We then review the behavioral nal, in this case a song, it does so under the expectation that the and neurophysiological work on conspecific song perception, signal will elicit a predictable (i.e. intended) behavior in the recei- focusing on individual vocal recognition mechanisms in European ver. Without the predictable correspondence between production starlings, a species of songbird. and perception, signals would lose their functionality. Thus, the presence of a functional signal implies a reliable correspondence between production and perception mechanisms shaped and 2. Perceptual psychoacoustics maintained by selection pressures. This correspondence confers a special status to communication signals. Like other natural stimuli, It is helpful for any description of a complex system to begin communication signals are often physically complex. Unlike most with a characterization of general abilities along fundamental complex natural stimuli, however, many of the physical dimen- dimensions. Common dimensions along which acoustic signals sions along which communication signals vary can be directly tied are deconstructed are frequency, amplitude, and time, and it is to adaptive behaviors. Research in oscine birds has capitalized on instructive to understand sensory processing at this level. The goal this idea to study the mechanisms underlying the perception and of such research is to inform our understanding of how more cognition of complex natural stimuli (song) in the context of natu- ‘atomic’ descriptions of sounds give rise to the perception of more ral behaviors. complex behaviorally relevant features. Such studies provide an What follows is an account of our current understanding about important context for studies of more complex signals, and estab- the ways in which the songbird auditory system interprets a con- lish the range over which any perceptual ability can operate. The following section provides a brief description of avian psycho- acoustics studies supporting the notion that humans and birds * Corresponding author. Address: UCSD, Department of Psychology, 9500 Gilman Dr. MC0109, La Jolla, CA 92093-0109, United States. experience a similar acoustic world. More thorough reviews are E-mail address: [email protected] (T.Q. Gentner). available (Dooling, 1982, 1992, 2000; Fay, 1988). 0093-934X/$ - see front matter Ó 2010 Elsevier Inc. All rights reserved. doi:10.1016/j.bandl.2009.09.008 60 D.P. Knudsen, T.Q. Gentner / Brain & Language 115 (2010) 59–68 In addition to hearing single tones, the auditory system must also discriminate between different tones. Understanding the min- imal detectable differences between tones can point to the types of frequency modulations within a signal that are available for a spe- cies to use in vocal communication. In general, birds are quite sen- sitive to changes in frequency, and can discriminate a change in frequency as small as 1% (Dooling, 1982), while humans have even lower detection thresholds across the range of audible frequencies. Birds’ sensitivity to frequency changes also depends on the type of frequency modulation and range of carrier frequencies (Lange- mann & Klump, 1992), results again similar to observations made in human studies (Demany & Semal, 1989; Fastl, 1978). To detect a change in intensity (loudness) between two successive tones, birds require a difference of about 3 dB, humans about 1 dB (Dool- ing, 1982). While humans have quantitatively lower detection thresholds for frequency and loudness discrimination, the similar- ity of findings in humans and birds point to auditory systems that are qualitatively similar in the range of psychophysically observa- ble spectral sensitivities. 2.2. Temporal sensitivity Most acoustic signals unfold over time, and processing in the temporal domain is therefore particularly important. Temporal processing abilities of songbirds have been studied in a variety of ways. A simple measure is the detectability of a sound as its tem- poral duration increases. In general, the longer the tone is played for, the lower the SPL needed for detection. Consistent with find- ings from a host of other animals including humans (see Brown & Maloney, 1986), birds’ thresholds for hearing a pure tone im- prove as the duration is increased from a few milliseconds to 200–300 ms (Dooling, 1980). Another common measure of tempo- ral acuity, known as the gap detection threshold, measures the minimum temporal interval that can be detected between two sounds. Several studies from birds show gap detection thresholds ranging from 2 to 3 ms, which is similar to thresholds found in hu- mans (see Klump & Maier, 1989). This suggests that intervals in natural vocalizations less than 2–3 ms may not be perceived. Dura- tion discrimination measures, which describe an organism’s ability to determine whether one sound has a longer duration than an- other, are also similar between birds and humans (Maier & Klump, 1990). 2.3. Masking Fig. 1. Functional auditory behaviors in songbirds. The gray boxes represent the functions that the auditory system must perform to mediate behavior. Text to the In psychoacoustics, the critical ratio describes the ability of an right of these functions gives examples of phenomena observed in songbirds (see organism to perceive a tone in a noisy background. It is defined text). Although this review focuses on songbird auditory processing, many of the as the SPL of a target tone needed for detection divided by the functions of the auditory system are likely conserved across a range of vertebrates, SPL of the background masking noise. Critical ratios are a function including humans. As behavioral complexity increases, so does the likelihood that particular mechanisms are unique to different species. The similarities and the of the frequency of the target tone, and in accordance with previ- differences between species yield powerful comparative hypotheses about the ous studies in humans and in other mammals, critical ratios in behavioral and neural mechanisms for auditory perception and cognition in most songbirds increase at about 3 dB per octave (Dooling et al., vertebrates. 1986; Langemann, Klump, & Dooling, 1995; Okanoya & Dooling, 1987). Most songbirds’ critical ratio curves show a similar shape 2.1. Spectral sensitivity to those of humans and other mammals, though humans show lowered threshold levels on the order of a few decibels (Okanoya Audibility curves, which describe the loudness (sound pressure & Dooling, 1987). level, SPL) required for detectability as a function of frequency, Comodulation masking release (CMR) is a slightly more com- have the same basic shape in many songbird species (Dooling, plex masking phenomenon that has been described in both birds Okanoya, Downing, & Hulse, 1986; Okanoya & Dooling, 1987). The and humans. CMR occurs when sounds that are modulated to- threshold sensitivity for pure tones in most songbird species is best gether across time serve to release each other from masking by around 2–5 kHz, increases gradually as the frequency of the tone overlapping noise. CMR is measured as the effective decrease in becomes lower, and increases quite sharply as the frequency of the threshold SPL afforded by the comodulation. CMR has been pro- tone rises. The typical high-frequency cutoff for songbirds is posed as mechanism for auditory stream segregation (discussed 8–11 kHz. Although audibility thresholds
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